The periodic rise in seawater temperature is one of the main environmental determinants of coral bleaching. However, the direct incidence of these episodic thermal anomalies on coral-associated microbiota and their subsequent effects on coral health are still not completely understood. In this study, we investigated the dynamics of three main microbial communities of the coral holobiont (e.g., Symbiodinium, bacteria and viruses), during an experimental thermal stress (+4 °C) conducted on the scleractinian Fungia repanda. The heat-treatment induced coral bleaching after 11 days and resulted in a final elevation of ca. 9, 130 and 250-fold in the abundance of mucosal viruses, bacteria, and Symbiodinium, respectively. On the contrary, the proportion of actively respiring bacterial cells declined by 95% in heat-stressed corals. The community composition of epibiotic bacteria in healthy corals also greatly differed from bleached ones, which also exhibited much higher production rates of viral epibionts. Overall, our results suggest that the shift in temperature induced a series of microbial changes, including the expulsion and transfer of Symbiodinium cells from the coral polyps to the mucus, the collapse of the physiological state of the native bacterial associates, a substantial alteration in their community structure, and accompanied by the development of a cortege of highly active virulent phages. Finally, this study provides new insights into the environmentally-driven microbial and viral processes responsible for the dislocation of the coral holobiont.